Abstract
Understanding the factors that modulate prokaryotic assemblages and their niche partitioning in marine environments is a longstanding challenge in marine microbial ecology. This study analyzes amplicon sequence variant (ASV) diversity and co-occurrence of prokaryotic (Archaea and Bacteria) communities through coastal-oceanic gradients in the NW Iberian upwelling system and adjacent open-ocean (Atlantic Ocean). Biogeographic patterns were investigated in relation with environmental conditions, mainly focusing on the optical signature of the dissolved organic matter (DOM). Alpha- and beta-diversity were horizontally homogeneous [with the only exception of Archaea (∼1700 m depth), attributed to the influence of Mediterranean water, MW], while beta-diversity was significantly vertically stratified. Prokaryotic communities were structured in four clusters (upper subsurface, lower subsurface, intermediate, and deep clusters). Deep (>2000 m) archaeal and bacterial assemblages, and intermediate (500-2000 m) Bacteria (mainly SAR202 and SAR406), were significantly related to humic-like DOM (FDOM-M), while intermediate Archaea were additionally related to biogeochemical attributes of the high-salinity signature of MW. Lower subsurface (100-500 m) Archaea (particularly one ASV belonging to the genus Candidatus Nitrosopelagicus) were mainly related to the imprint of high-salinity MW, while upper subsurface (≤100 m) archaeal assemblages (particularly some ASVs belonging to Marine Group II) were linked to protein-like DOM (aCDOM254). Conversely, both upper and lower subsurface bacterial assemblages were mainly linked to aCDOM254 (particularly ASVs belonging to Rhodobacteraceae, Cyanobacteria, and Flavobacteriaceae) and nitrite concentration (mainly members of Planctomycetes). Most importantly, our analysis unveiled depth-ecotypes, such as the ASVs MarG.II_1 belonging to the archaeal deep cluster (linked to FDOM-M) and MarG.II_2 belonging to the upper subsurface cluster (related to FDOM-T and aCDOM254). This result strongly suggests DOM-mediated vertical niche differentiation, with further implications for ecosystem functioning. Similarly, positive and negative co-occurrence relationships also suggested niche partitioning (e.g., between the closely related ASVs Thaum._Nit._Nit._Nit._1 and _2) and competitive exclusion (e.g., between Thaum._Nit._Nit._Nit._4 and _5), supporting the finding of non-randomly, vertically structured prokaryotic communities. Overall, differences between Archaea and Bacteria and among closely related ASVs were revealed in their preferential relationship with compositional changes in the DOM pool and environmental forcing. Our results provide new insights on the ecological processes shaping prokaryotic assembly and biogeography.
Highlights
Marine heterotrophic microbes depend upon dissolved organic matter (DOM) quantity and quality to fulfill their metabolic requirements, as they recycle dissolved organic carbon through the microbial loop (Azam et al, 1983)
The squared Brunt-Väissälä frequency (N2) profiles (Supplementary Figure 4) revealed stratified conditions in the upper water column, with maximum stratification underneath the mixed layer depth, which was shallow along the two transects (∼5 m at coastal stations, increasing up to only >20 m at offshore stations and station 62 in the Santander section), and above ∼100 m depth
A significant vertical niche partitioning was revealed for Archaea and Bacteria assemblages, related to the vertical variability in environmental conditions (DOM quality and quantity and hydrography)
Summary
Marine heterotrophic microbes depend upon dissolved organic matter (DOM) quantity and quality to fulfill their metabolic requirements, as they recycle dissolved organic carbon through the microbial loop (Azam et al, 1983). Concurrent data about prokaryotic diversity and DOM quantity and quality indicators are extraordinarily scarce in oceanographic surveys (DobalAmador et al, 2016; Guerrero-Feijóo et al, 2017), so virtually all the available information comes from mesocosm and/or experimental approaches (e.g., Omori et al, 2020; Varela et al, 2020; Gutiérrez-Barral et al, 2021). These empirical methods are of great value since they provide important information on the behavior of different populations under controlled conditions. Their results are only cautiously comparable with natural populations due to the so-called “bottle effect” (Zobell and Anderson, 1936)
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